Transmission of Batrachochytrium dendrobatidis to wood frogs (Lithobates sylvaticus) via a bullfrog (L. catesbeianus) vector

Chytridiomycosis, an emerging infectious disease caused by the chytrid fungus Batrachochytrium dendrobatidis, threatens anuran populations worldwide. Effects of B. dendrobatidis on frog species are variable. Some species typically develop nonlethal infections and may function as carriers; others typically develop lethal infections that can lead to population declines. Nonlethal infections in the bullfrog (Lithobates catesbeianus) are well-documented. In contrast, recently metamorphosed wood frogs (L. sylvaticus) can die from chytridiomycosis. We conducted an ex-situ experiment between May and July 2010 to determine whether B. dendrobatidis-infected bullfrogs could transmit the fungus to wood frog tadpoles when the two species shared a body of water. We tested for B. dendrobatidis infections with quantitative polymerase chain reactions (qPCR) in a subsample of the wood frog tadpoles and in all metamorphosed wood frogs and compared risk of death of froglets exposed and unexposed to infected bullfrogs. We detected B. dendrobatidis sporadically in subsampled treatment tadpoles (nine of 90, 10%) and frequently in treatment froglets (112 of 113, 99.1%). Pooled risk of froglet death was higher (P<0.001) in treatment enclosures than in control enclosures. Our results indicate that, at the low infection loads bullfrogs tend to carry, swabbing for PCR analyses may underestimate prevalence of B. dendrobatidis in this species. We highlight bullfrog disease screening as a management challenge, especially in light of exotic bullfrog colonies on multiple continents and large-scale global trade in this species. We document the importance of quantifying lethal and sublethal effects of bullfrog vectors on B. dendrobatidis-susceptible species.     

Amphibian richness patterns in Atlantic Forest areas invaded by American bullfrogs

The relationship between invasion success and native biodiversity is central to biological invasion research. New theoretical and analytical approaches have revealed that spatial scale, land‐use factors and community assemblages are important predictors of the relationship between community diversity and invasibility and the negative effects of invasive species on community diversity. In this study we assess if the abundance of Lithobates catesbeianus, the American bullfrog, negatively affects the richness of native amphibian species in Atlantic Forest waterbodies in Brazil. Although this species has been invading Atlantic Forest areas since the 1930s, studies that estimate the invasion effects upon native species diversity are lacking. We developed a model to understand the impact of environmental, spatial and species composition gradients on the relationships between bullfrogs and native species richness. We found a weak positive relationship between bullfrog abundance and species richness in invaded areas. The path model revealed that this is an indirect relationship mediated by community composition gradients. Our results indicate that bullfrogs are more abundant in certain amphibian communities, which can be species‐rich. Local factors describing habitat heterogeneity were the main predictors of amphibian species richness and composition and bullfrog abundance. Our results reinforce the important role of habitats in determining both native species diversity and potential invasibility.     

浙江东部牛蛙的自然种群及潜在危害

牛蛙(Rana catesbeiana)的入侵已成为一些本地两栖类种群数量下降或灭绝的主要因素之一。1959年牛蛙被引入中国大陆,但直到1990年才开始在国内大范围饲养。牛蛙的自然种群在国内一直未见报道。我们于2003年9—11月调查了浙江省东部5区3县的牛蛙种群,发现在岱山、秀山、六横及佛渡岛上有牛蛙分布,共捕获23只牛蛙,包括4只成年个体,18个亚成体和1只蝌蚪。于2004年1月和2月在岱山捕获28只蝌蚪。结果显示：(1)牛蛙的蝌蚪能在当地越冬成活,说明牛蛙在上述4岛成功地建立了自然种群;(2)牛蛙主要分布于水库、池塘和溪流,牛蛙的生境与6种当地蛙有部分重叠;(3)养殖时管理不善造成的牛蛙逃逸,以及牛蛙价格过低而导致养殖户将牛蛙弃置野外可能是牛蛙入侵的主要原因。牛蛙对当地蛙的潜在威胁很大,开展牛蛙的分布、食性和种群动态研究是当务之急。     

Multiple predator effects on size-dependent behavior and mortality of two species of anuran larvae

This study examined the effects of multiple predators on size‐specific behavior and mortality of two species of anuran larvae. Particularly, we focused on how trait changes in predators and prey may be transmitted to other species in the food web. In laboratory experiments, we examined the effects of bluegill sunfish, Lepomis macrochirus, and the odonate larva Anax junius on behavior and mortality of tadpoles of the bullfrog, Rana catesbeiana, and the green frog R. clamitans. Experiments were conducted with predators alone and together to assess effects on behavior and mortality of the tadpoles. The experiments were replicated on five size classes of the tadpoles to evaluate how responses varied with body size.
Predation rates by Anax were higher on bullfrogs than on green frogs, and both bullfrogs and green frogs suffered greater mortality from Anax than from bluegill. Bluegill only consumed green frogs. Predation rates by both predators decreased with increasing tadpole size and decreased in the non‐lethal (caged) presence of the other predator. Both anuran larvae decreased activity when exposed to predators. Bullfrogs, however, decreased activity more in the presence of Anax than in the presence of bluegill, whereas green frogs decreased activity similarly in the presence of both predators. The largest size class of green frogs, but not of bullfrogs, exhibited spatial avoidance of bluegill. These responses were directly related to the risk posed by the different predators to each anuran species. Anax activity (speed and move frequency) also was higher when alone than in the non‐lethal presence of bluegill. We observed decreased predation rate of each predator in the non‐lethal presence of the other, apparently caused by two different mechanisms. Bluegill decreased Anax mortality on tadpoles by restricting the Anax activity. In contrast, Anax decreased bluegill mortality on tadpoles by reducing tadpole activity. We discuss how the activity and spatial responses of the tadpoles interact with palatability and body size to create different mortality patterns in the prey species and the implications of these results to direct and indirect interactions in this system.     

Foraging Responses of the Larvae of Invasive Bullfrogs(Lithobates catesbeianus): Possible Implications for Bullfrog Control and Ecological Impact in China

The predatory behavior of invasive species can affect their ecological impact, and offer opportunities for targeted control. In Australia, tadpoles of invasive cane toads(Rhinella marina) do not consume eggs of native anurans, but are strongly attracted to(and consume) newly-laid eggs of conspecifics; chemical cues from such eggs(or adult secretions) thus can be used to attract toad tadpoles to traps. Do other invasive anurans show similar selectivity? Our laboratory trials on a Chinese population of invasive American bullfrogs(Lithobates catesbeianus) revealed similar behaviors as exhibited by Australian cane toads. Bullfrog tadpoles rarely consumed the eggs of native anurans, but were attracted to both bullfrog eggs and bullfrog skin secretions. Although the attraction response was less intense in bullfrogs than in cane toads, it might nonetheless enable selective removal of bullfrog tadpoles from invaded sites.     

Diet and Prey Selection of the Invasive American Bullfrog(Lithobates catesbeianus) in Southwestern China

Invasive predators have been widely regarded as one of the principle drivers of the global decline of amphibians, which are among the most threatened vertebrate taxon on Earth. The American bullfrog(Lithobates catesbeianus) is identified as one of the most successful vertebrate invaders and has caused the decline or extinction of some native amphibians in many regions and countries including China. Based on field surveys and stomach content analyses, we examined the diet composition of the invasive bullfrog for the first time in two invaded populations in Yunnan Province, southwestern China, a region of global conservation priority, during the breeding season from 2008 to 2014. Additionally, we conducted the first quantitative study on the prey selection of this global invader among their invaded ranges after controlling for the local anuran assemblage and other aquatic preys in the environment. Our results showed that the range of food items in the stomachs of bullfrogs spanned more than 30 species belonging to ten taxonomic classes. Both of post-metamorphosis individuals and juveniles preyed upon native frogs, independent of the bullfrog's body size and mouth width. Importantly, Jacobs' selection index showed a bullfrog preference for the Yunnan pond frog(Babina pleuraden), one native endemic anuran with population decline, in terms of both food volume and occurrence. We therefore provided direct evidence on the predation impact of the invasive bullfrog on an endemic anuran and urged further efforts to prevent the dispersal of this invader into more fragile habitats to reduce their negative impacts on native amphibians.     

Population genetics of introduced bullfrogs, Rana (Lithobates) catesbeianus, in the Willamette Valley, Oregon, USA

The American bullfrog, Rana (Lithobates) catesbeianus, is endemic to eastern North America, but has been introduced to approximately 40 countries on four continents and is considered one of the hundred worst invasive alien species in the world. Here, we investigated the genetics of invasive bullfrogs in the Willamette Valley, Oregon, USA, where bullfrogs are widespread and abundant to determine: (1) the minimum number of bullfrog introductions; (2) the native source population(s); and (3) whether genetic variation is reduced compared to source populations. To answer these questions, we analyzed partial sequences of the mitochondrial cytochrome b gene for 251 bullfrogs from the Willamette Valley and the native range. We found that bullfrogs from the Mississippi River basin and Great Lakes region were introduced at least once to the Willamette Valley. Genetic variation measured as haplotype diversity (h) and nucleotide diversity (?? _n ) was not significantly different between Willamette Valley and source populations. Our results were in contrast to a recent genetic analysis of invasive bullfrog populations in Europe, which found that genetic variation in European bullfrog populations was much lower than in source populations. European bullfrogs also originated from different source populations than Willamette Valley bullfrogs. The difference in genetic composition between Willamette Valley and European bullfrogs is likely due to differences in their invasion histories and may have implications for the potential of bullfrogs in these different regions to adapt and expand.     

Bullfrog (<Emphasis Type="Italic">Lithobates catesbeianus</Emphasis>) invasion in Uruguay

This is the first report of North American bullfrogs, Lithobates catesbeianus (=Rana catesbeiana), invasion in Uruguay. This Anura was introduced for farming proposes in 1987, but at present most of the farms are closed. At one of these closed farms, located at Rincón de Pando, Canelones, we report the occurrence of a feral population of L. catesbeianus. This invasion point is at an early stage and restricted to one or two ponds. We also report the effects of L. catesbeianus invasion in the community structure. This includes species composition and species size structure. In this system bullfrog tadpoles constitute a very important proportion of the present biomass. Bullfrog tadpoles appear to be displacing native amphibians and having some type of positive interaction with fishes. At the invaded system we found more fish species and larger sizes of the shared fish species. We analyze the involved risks of this invasion, the ecological impact by predation, the competition and habitat modification, and the potential of bullfrog to act as pathogens vector. We also recommend taking measures in order to avoid the expansion of this population. There is also the need of studies to search for new invasion points in Uruguay, especially where bullfrog farms were located.     

Extracts of the invasive shrub Lonicera maackii increase mortality and alter behavior of amphibian larvae

Water-soluble phytochemicals produced by invasive plants may represent novel elements of invaded ecosystems that can precipitate a variety of direct and indirect effects on native organisms. Phenolic compounds in particular are a common plant defense, and these compounds may have disproportionate impacts on amphibians compared to other taxa. We coupled an exploration of invasive plant extract effects on larvae of four amphibian species (the salamander Ambystoma maculatum, the toad Anaxyrus americanus, and the frogs Hyla sp. and Lithobates blairi) with behavioral observations designed to determine whether behavior can ameliorate the negative effects of exposure to invasive plant extracts. Larvae were reared in extracts of the widespread invasive Amur honeysuckle (Lonicera maackii), mixed native leaf litter, and a water control. Anaxyrus americanus tadpoles reared in L. maackii extracts were more likely to die than tadpoles reared in native extracts, but differences in mortality following rearing in native and exotic extracts were not significant for the other three species. Anaxyrus americanus and L. blairi tadpoles made more trips to the surface in L. maackii extracts than in native extracts, consistent with the hypothesis that exotic extracts may interfere with respiratory physiology and suggesting that L. blairi can behaviorally ameliorate the negative effects of L. maackii extracts. Our study highlights both a direct and indirect pathway by which invasive plant extracts may alter the ecological dynamics of native fauna.     

Behavioral responses of American toad and bullfrog tadpoles to the presence of cues from the invasive fish, Gambusia affinis

The introduction of non-native predators is thought to have important negative effects on native prey populations. The susceptibility of native prey to non-native or introduced predators may depend on their ability to respond appropriately to the presence of these non-native predators. We conducted a laboratory based behavioral experiment to examine the response of American toad (Bufo americanus) and bullfrog (Rana catesbeiana) tadpoles to the presence of cues from the introduced mosquitofish (Gambusia affinis), a potential tadpole predator. Neither the American toad tadpoles nor the bullfrog tadpoles responded behaviorally to the presence of mosquitofish cues. If tadpoles are unable to respond to the presence of mosquitofish cues appropriately, then their ability to avoid predation by mosquitofish may be compromised and this may contribute to the impacts of mosquitofish on some tadpole populations.     

A review of ecological interactions between native frogs and invasive cane toads in Australia

Translocated from their native range in the Americas in 1935, cane toads (Rhinella marina, Bufonidae) have now spread through much of tropical and subtropical Australia. The toad's invasion and impact have attracted detailed study. In this paper, I review information on ecological interactions between cane toads and Australian anurans. The phylogenetic relatedness and ecological similarity between frogs and toads creates opportunities for diverse interactions, ranging from predation to competition to parasite transfer, plus a host of indirect effects mediated via impacts of toads on other species, and by people's attempts to control toads. The most clear‐cut effect of toads on frogs is a positive one: reducing predator pressure by fatally poisoning anuran‐eating varanid lizards. However, toads also have a wide range of other effects on frogs, some positive (e.g. taking up parasites that would otherwise infect native frogs) and others negative (e.g. eating frogs, poisoning frogs, competing with tadpoles). Although information on such mechanisms predicts intense interactions between toads and frogs, field surveys show that cane toad invasion has negligible overall impacts on frog abundance. That counter‐intuitive result is because of a broad balancing of negative and positive impacts, coupled with stochastic (weather‐induced) fluctuations in anuran abundance that overwhelm any impacts of toads. Also, the impacts of toads on frogs differ among frog species and life‐history stages, and depend upon local environmental conditions. The impacts of native frogs on cane toads have attracted much less study, but may well be important: frogs may impose biotic resistance to cane toad colonization, especially via competition in the larval phase. Overall, the interactions between native frogs and invasive toads illustrate the diverse ways in which an invader's arrival can perturb the native fauna by both direct and indirect mechanisms, and by which the native species can curtail an invader's success. These studies also offer a cautionary tale about the difficulty of predicting the impact of an invasive species, even with a clear understanding of mechanisms of direct interaction.     

The Ability of Three Species of Tadpoles to Differentiate among Potential Fish Predators

The ability of prey to respond to novel predator cues may depend on the generality or specificity of the response to predator cues. We used laboratory behavioral experiments to examine the ability of tadpoles of three species of anurans (American toad, Bufo americanus ; bullfrog, Rana catesbeiana ; and green frog, R. clamitans ) to respond to the presence of two native potential predators (bluegill, Lepomis macrochirus ; and largemouth bass, Micropterus salmoides ) and one non-native potential predator (goldfish, Carassius auratus ). We also examined the effect of tadpole size on the behavioral responses of American toads and green frogs to predator cues. All three species of tadpoles responded to the presence of predator cues, although the specific responses varied among species. American toads and green frogs reduced activity in the presence of at least some fish cues, but bullfrog tadpoles did not change their activity. Bullfrogs decreased use of vegetation in the presence of some predator cues, whereas American toads and green frogs did not. American toads only responded to the presence of bluegill cues but not the other fish predator cues, whereas bullfrogs and green frogs responded more generally to the fish predators. In both American toads and green frogs, tadpole size affected behavior. For American toads, activity increased, as did the use of the vegetated side of the aquarium, in larger tadpoles. Not only did size affect American toad behavior, but it also influenced the responses of the tadpoles to predator cues. For green frogs, activity decreased in larger tadpoles. Our results suggest that behavioral responses of tadpoles to predator cues can be influenced by both the identity of the predator and the prey, as well as the size of the potential prey.     

Prediction and validation of the potential global distribution of a problematic alien invasive species — the American bullfrog

Predicting the probability of successful establishment and invasion of alien species at global scale, by matching climatic and land use data, is a priority for the risk assessment. Both large- and local-scale factors contribute to the outcome of invasions, and should be integrated to improve the predictions. At global scale, we used climatic and land use layers to evaluate the habitat suitability for the American bullfrog Rana catesbeiana , a major invasive species that is among the causes of amphibian decline. Environmental models were built by using Maxent, a machine learning method. Then, we integrated global data with information on richness of native communities and hunting pressure collected at the local scale. Global-scale data allowed us to delineate the areas with the highest suitability for this species. Predicted suitability was significantly related to the invasiveness observed for bullfrog populations historically introduced in Europe, but did not explain a large portion of variability in invasion success. The integration of data at the global and local scales greatly improved the performance of models, and explained > 57% of the variance in introduction success: bullfrogs were more invasive in areas with high suitability and low hunting pressure over frogs. Our study identified the climatic factors entailing the risk of invasion by bullfrogs, and stresses the importance of the integration of biotic and abiotic data collected at different spatial scales, to evaluate the areas where monitoring and management efforts need to be focused.     

Invasive North American bullfrogs transmit lethal fungus <Emphasis Type="Italic">Batrachochytrium dendrobatidis</Emphasis> infections to native amphibian host species

Invasive species can be a threat to native species in several ways, including transmitting lethal infections caused by the parasites they carry. However, invasive species may also be plagued by novel and lethal infections they acquire when invading, making inferences regarding the ability of an invasive host to vector disease difficult from field observations of infection and disease. This is the case for the pathogenic fungus Batrachochytrium dendrobatidis (Bd) in Europe and one invasive host species, the North American bullfrog Lithobates catesbeianus, hypothesized to be responsible for vectoring lethal infection to European native amphibians. We tested this hypothesis experimentally using the alpine newt Ichthyosaura alpestris as our model native host. Our results show that infected bullfrog tadpoles are effective vectors of Bd. Native adult newts co-housed with experimentally infected bullfrog tadpoles became Bd infected (molecular and histological tests). Moreover, the exposed adult newts suffered mortality while the majority of infected bullfrog tadpoles survived until metamorphosis. These results cannot resolve the historical role of alien species in establishing the distribution of Bd across Europe or other regions in the world where this species was introduced, but they show its potential role as a Bd reservoir capable of transmitting lethal infections to native amphibians. Finally, our results also suggest that the removal of infected bullfrogs from aquatic environments may serve to reduce the availability of Bd in European amphibian communities, offering another justification for bullfrog eradication programmes that are currently underway or may be considered.     

Competing tadpoles: Australian native frogs affect invasive cane toads (Rhinella marina) in natural waterbodies

The cane toad (Rhinella marina) is one of the most successful invasive species worldwide, and has caused significant negative impacts on Australian fauna. Experimental work in the laboratory and in mesocosms has shown that tadpoles of native frogs can affect survival, size at metamorphosis and duration of larval period of cane toad tadpoles. To test if these effects occur in nature, we conducted a field experiment using two temporary ponds where we set up enclosures with tadpoles of native green tree frogs (Litoria caerulea) and cane toads in treatments with a range of densities and combinations. The presence of green tree frog tadpoles significantly decreased the growth rate of toad tadpoles and increased the duration of their larval period in both ponds; in one pond, frog tadpoles also significantly reduced the body length and mass of metamorph toads. Toad tadpoles did not have any significant negative effects on green tree frog tadpoles, but there was strong intraspecific competition within the latter species: increased frog tadpole density resulted in increased larval period and reduced survival, growth rate and size at metamorphosis for frogs at one or both ponds. Our results are encouraging for the possibility of using native frogs as one component of an integrated approach to the biological control of cane toads.     

Direct and indirect effects of the introduced toad Bufo marinus (Anura: Bufonidae) on populations of native anuran larvae in Australia

Introduced species are frequently believed to have adverse effects on native biota and ecosystems. However, much of our knowledge of the ecological impacts of introduced species is anecdotal, and the mechanisms controlling these effects are often poorly understood. I used replicated artificial pond experiments to investigate the impact of eggs and hatchlings of the introduced toad Bufo marinus on populations of native anuran larvae (Limnodynastes ornatus and Litoria rubella) in Australia. Bufo marinus eggs and hatchlings are highly toxic to predatory native tadpoles. Under naturalistic conditions, populations of predatory L. ornatus tadpoles experienced significantly reduced survival when exposed to Bufo eggs and hatchlings. The impact of Bufo on L. ornatus survival was positively correlated with Bufo density. However, the toxic effects of Bufo on L. ornatus indirectly facilitated the survival of later-breeding L. rubella by altering predator-prey interactions between L. ornatus and L. rubella. Limnodynastes ornatus tadpoles are voracious predators of L. rubella eggs and hatchlings. Consequently, the negative impact of Bufo on populations of L. ornatus tadpoles reduced the intensity of predation by L. ornatus tadpoles on L. rubella eggs and hatchlings, thereby increasing L. rubella survival. The results demonstrate that B. marinus plays an important role in structuring native larval anuran communities via direct and indirect mechanisms, and that Bufo may have both negative and positive effects on populations of native anuran larvae. As far as I am aware, these are the first quantitative data to demonstrate that introduced fauna may affect populations of native biota via toxic effects.     

Antipredator Behavioral Responses of Native and Exotic Tadpoles to Novel Predator

Factors related to the invasion process, such as high abundance of invaders, residence time, and functional distinctiveness, are well documented, but less attention has been given to the effects of antipredator strategy of invasive species during colonization. In this study, we explored the antipredator strategy of an introduced species by comparing the predator avoidance behaviors of two native anuran species and one introduced("exotic") species in the presence of different predators. The two native anuran species used in the study were Black-spotted Pond Frog Rana nigromaculata and Terrestrial Frog Rana limnocharis. The introduced(invasive) species used was American bullfrog Lithobates catesbeianus. Chinese pond turtle Chinemys reevesii, Red-backed rat snake Elaphe rufodorsata, and Big-headed turtle Platysternon megacephalum were used as predator species. Chinese pond turtles and Red-backed rat snakes are native predators of Black-spotted Pond Frogs and Terrestrial Frogs, while Big-headed turtles are novel("unfamiliar") to the two frogs. All three predator species are novel("unfamiliar") to the American bullfrog. The results show that tadpoles of the two native species displayed behaviors of recognizing the two native predators, but did not display the capability of identifying the novel predator. Results from our study also suggest that American bullfrog tadpoles exhibited strong antipredator behavioral responses by displaying the capability of identifying "unfamiliar" predators without cohabitation history and prior exposure to them. Such antipredator behavioral responses could have resulted in more favorable outcomes for an invading species during the invasive introductory process.     

An exotic species is the favorite prey of a native enemy

Although native enemies in an exotic species'' new range are considered to affect its ability to invade, few studies have evaluated predation pressures from native enemies on exotic species in their new range. The exotic prey naiveté hypothesis (EPNH) states that exotic species may be at a disadvantage because of its naïveté towards native enemies and, therefore, may suffer higher predation pressures from the enemy than native prey species. Corollaries of this hypothesis include the native enemy preferring exotic species over native species and the diet of the enemy being influenced by the abundance of the exotic species. We comprehensively tested this hypothesis using introduced North American bullfrogs (Lithobates catesbeianus, referred to as bullfrog), a native red-banded snake (Dinodon rufozonatum, the enemy) and four native anuran species in permanent still water bodies as a model system in Daishan, China. We investigated reciprocal recognition between snakes and anuran species (bullfrogs and three common native species) and the diet preference of the snakes for bullfrogs and the three species in laboratory experiments, and the diet preference and bullfrog density in the wild. Bullfrogs are naive to the snakes, but the native anurans are not. However, the snakes can identify bullfrogs as prey, and in fact, prefer bullfrogs over the native anurans in manipulative experiments with and without a control for body size and in the wild, indicating that bullfrogs are subjected to higher predation pressures from the snakes than the native species. The proportion of bullfrogs in the snakes'' diet is positively correlated with the abundance of bullfrogs in the wild. Our results provide strong evidence for the EPNH. The results highlight the biological resistance of native enemies to naïve exotic species.     

Invasion of the acoustic niche: variable responses by native species to invasive American bullfrog calls

Biological invasions are a major threat to biodiversity. Invasive species that use acoustic communication can affect native species through interference in the acoustic niche. The American Bullfrog Lithobates catesbeianus is a highly invasive anuran that is widely distributed in the Brazilian Atlantic Rainforest. Adult male bullfrogs emit loud advertisement calls at frequencies that overlap with the calls of several native species of frogs. Given that spectral overlap is a major factor in acoustic masking, the purpose of this study was to test the effects of the acoustic invasion of L. catesbeianus on native frogs that have calls with and without spectral overlap with the invader. In field experiments, we exposed calling males of two overlapping species and two non-overlapping species to recorded bullfrog vocalizations, white noise, and the vocalization of another native frog species. To identify effects, we compared calls recorded before, during, and after exposure. Our results showed that native species altered their calls in response to the bullfrog calls. However, we also observed similar responses to white noise and heterospecific native calls. Both the invasive and heterospecific calls were emitted at low frequencies, which suggests that the observed responses might be specific to low-frequency calls. Our results provide evidence that the introduction of new sounds can cause native species to modify their calls, and that responses to exogenous sounds are species- and stimulus-specific.     

Indirect ecological impacts of an invasive toad on predator–prey interactions among native species

One of the many ways that invasive species can affect native ecosystems is by modifying the behavioural and ecological interactions among native species. For example, the arrival of the highly toxic cane toad (Bufo marinus) in tropical Australia has induced toad-aversion in some native predators. Has that shift also affected the predators’ responses to native prey—for example, by reducing vulnerability of native tadpoles via a mimicry effect, or increasing vulnerability of other prey types (such as insects) via a shift in predator feeding tactics? We exposed a native predator (northern trout gudgeon, Mogurnda mogurnda) to toad tadpoles in the laboratory, and measured effects of that exposure on the fish’s subsequent intake of native tadpoles and crickets. As predicted, toad-exposed fishes reduced their rate of predation on (palatable) tadpoles of native frogs (Litoria caerulea and L. nasuta). If alternative prey (crickets) were available also, the toad-exposed fishes shifted even more strongly away from predation on native tadpoles. Thus, invasion of a toxic species can provide a mimicry benefit to native taxa that resemble the invader, and can shift predation pressure onto other taxa.